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A Subgeneric Classification of Selaginella (Selaginellaceae)

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A Subgeneric Classification of Selaginella (Selaginellaceae) RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY A subgeneric classifi cation of Selaginella (Selaginellaceae)1 Stina Weststrand and Petra Korall2 PREMISE OF THE STUDY: The lycophyte family Selaginellaceae includes approximately 750 herbaceous species worldwide, with the main species richness in the tropics and subtropics. We recently presented a phylogenetic analysis of Selaginellaceae based on DNA sequence data and, with the phylogeny as a framework, the study discussed the character evolution of the group focusing on gross morphology. Here we translate these fi ndings into a new classifi cation. METHODS: To present a robust and useful classifi cation, we identifi ed well-supported monophyletic groups from our previous phylogenetic analysis of 223 species, which together represent the diversity of the family with respect to morphology, taxonomy, and geographical distribution. Care was taken to choose groups with supporting morphology. KEY RESULTS: In this classifi cation, we recognize a single genus Selaginella and seven subgenera: Selaginella , Rupestrae , Lepidophyllae , Gymnogynum , Exal- tatae , Ericetorum , and Stachygynandrum . The subgenera are all well supported based on analysis of DNA sequence data and morphology. A key to the subgenera is presented. CONCLUSIONS: Our new classifi cation is based on a well-founded hypothesis of the evolutionary relationships of Selaginella , and each subgenus can be identifi ed by a suite of morphological features, most of them possible to study in the fi eld. Our intention is that the classifi cation will be useful not only to experts in the fi eld, but also to a broader audience. KEY WORDS classifi cation; key; lycophytes; morphology; phylogeny; Selaginellaceae; subgenera Th e phylogeny of Selaginellaceae Willk., one of three lycophyte Jermy, 1986 ), divided the species into two to several genera (e.g., families, was addressed in a companion article in this issue Palisot de Beauvois, 1804 ; Rothmaler, 1944 ; Soják, 1993 ; Tzvelev, ( Weststrand and Korall, 2016 ) and has been the subject of much 2004 ), or even included all species as subgenera under Lycopodium attention in the last 15 years (e.g., Korall et al., 1999 ; Korall and L. ( Reichenbach, 1828 ), see Zhou and Zhang (2015) for a historical Kenrick, 2002 , 2004 ; Arrigo et al., 2013 ; Zhou et al., 2015c ). In that review. Th e classifi cation most oft en referred to during the last de- large-scale study, we analyzed plastid and single-copy nuclear cades is the one published by Jermy (1986) . He recognized a single data from approximately one-third of the 750 species ( Jermy, genus Selaginella with fi ve subgenera: Selaginella (2 species), 1990 ) and discussed the morphological evolution of the group. Tetragonostachys Jermy (ca. 50 species), Ericetorum Jermy (3 spe- Here we present a new classifi cation of Selaginellaceae, based on cies), Heterostachys Baker (ca. 60 species), and Stachygynandrum these results. (P.Beauv. ex Mirb.) Baker (ca. 600 species). Morphological features Th e genus Selaginella was fi rst described by Palisot de Beauvois used to distinguish groups in classifi cations were, e.g., isophylly vs. in 1804 . Since then, a number of classifi cations have been proposed anisophylly, phyllotaxy, habit, stelar arrangement, and spore orna- that either recognized a single genus Selaginella P.Beauv. (e.g., mentation. Phylogenetic studies of the group have shown that these Spring, 1840 , 1849 ; Braun, 1858 ; Baker, 1883 ; Hieronymus and characters (as they have been defi ned) oft en are homoplastic, in- Sadebeck, 1901 ; Walton and Alston, 1938 ; Tryon and Tryon, 1982 ; volving reversals and/or parallelisms, and that none of these mor- phology-based classifi cations properly refl ect the phylogeny of the 1 Manuscript received 8 April 2016; revision accepted 30 September 2016. group ( Korall and Kenrick, 2002 ; Zhou et al., 2015c ; Weststrand Systematic Biology, Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden and Korall, 2016 ). In 2015, Zhou and Zhang published the fi rst clas- 2 Author for correspondence (e-mail: [email protected]) sifi cation based on a phylogenetic analysis of the group ( Zhou et al., doi:10.3732/ajb.1600288 2015c ). On the basis of this study, in combination with morphological 2160 • AMERICAN JOURNAL OF BOTANY 103 (12): 2160 – 2169 , 2016; http://www.amjbot.org/ © 2016 Weststrand and Korall. Published by the Botanical Society of America. This work is licensed under a Creative Commons Attribution License (CC-BY 4.0). DECEMBER 2016 , VOLUME 103 • WESTSTRAND AND KORALL—SUBGENERIC CLASSIFICATION OF SELAGINELLA • 2161 and chromosome data ( Zhou et al., 2015c ), Zhou and Zhang (2015) 1901 ; Steel, 1923 ). However, rhizophore development is complex recognized six subgenera and 18 sections within the single genus and variable, and this division into rhizophore positions does not Selaginella . fully refl ect the variation observed. More comparative studies are Selaginellaceae, with the single genus Selaginella , is widely dis- needed for a full understanding (but see, e.g., Webster and Steeves, tributed throughout the world, from arctic and alpine regions to 1964 ; Lu and Jernstedt, 1996 ; and references therein). Th e stems of the tropics and subtropics, where the main species diversity is some species have articulations below stem dichotomies; these are found ( Jermy, 1990 ). Th e species are herbaceous and range from swellings that in dried specimens oft en are seen as dark constricted creeping, sometimes mat-forming, to erect, and occasionally long segments ( Jermy, 1990 ). Th e stem stele is a protostele, which in and scandent. Approximately 50 species, most of them found in most species is a simple, circular to elliptic monostele, but bistelic, temperate and dry areas of the world, have vegetative leaves that are tristelic, or polystelic arrangements are also relatively common monomorphic ( Jermy, 1990 ). Th ese have helically arranged leaves, (e.g., Harvey-Gibson, 1894 ; Hieronymus and Sadebeck, 1901 ). except for three species where the leaves are decussately arranged Lobed protostelic forms (actinostele or actino-plectostele) are [ Selaginella gracillima (Kunze) Spring ex Salomon, S. pygmaea found in a few species (e.g., Wardlaw, 1925 ; Mickel and Hellwig, (Kaulf.) Alston, and S. uliginosa (Labill.) Spring] ( Jermy, 1986 ). 1969 ; Weststrand and Korall, 2016 ). A few species also have a sole- However, the majority of Selaginella species, most of them found in nostelic rhizome (e.g., Harvey-Gibson, 1894 ; Steel, 1923 ). warm and humid regions, have dimorphic vegetative leaves. Th e Our knowledge of the phylogenetic relationships of Selaginella- anisophyllous shoots have leaves in four rows with two rows of ceae has increased signifi cantly since the fi rst phylogenetic analysis smaller leaves on the upper, dorsal side of the shoot, and two rows was published in 1999 ( Korall et al., 1999 ). Our study in this issue of larger leaves on the lower, ventral side ( Jermy, 1990 ; see fi g. 3 of ( Weststrand and Korall, 2016 ) showed, based on 223 species, an Korall and Kenrick, 2002 ). overall well-resolved and well-supported phylogeny. Th e resulting Selaginellaceae is heterosporous, a synapomorphy shared with topology is in concordance with previously published phylogenetic the sister lineage Isoëtaceae Dumort. ( Jermy, 1990 ; Wikström and analyses of the group ( Korall et al., 1999 ; Korall and Kenrick, 2002 , Kenrick, 1997 ; Korall et al., 1999 ). Th e mega- and microsporangia, 2004 ; Arrigo et al., 2013 ; Zhou et al., 2015c ). Together, the diff erent enclosing mega- and microspores, respectively, are subtended by studies show that Selaginellaceae is supported as monophyletic and sporophylls and arranged in strobili at branch tips ( Jermy, 1990 ; with that a clade of two species (the isophyllous S. selaginoides and S. a few exceptions, see, e.g., Valdespino et al., 2015 ). Th e strobili are, defl exa ) is sister to the rhizophoric clade, including all other taxa like the vegetative shoots, either isophyllous or anisophyllous. Iso- ( Fig. 1 ) . Th e rhizophoric clade is supported by two morphological phyllous strobili are most common and found in all species with iso- synapomorphies: presence of rhizophores and tetrastichous stro- phyllous vegetative shoots, as well as in the majority of species with bili. Th e fi rst divergence in the rhizophoric clade gives rise to clades anisophyllous vegetative shoots ( Jermy, 1990 ). Th e sporophylls are in A and B. Clade B and fi ve major subclades within clade A can each tetrastichous strobili in all but two species, the type S. selaginoides be identifi ed based on a suite of morphological features ( Weststrand (L.) P.Beauv. ex Schrank & Mart. and S. defl exa Brack., where they and Korall, 2016 ). are helically arranged ( Jermy, 1986 ). Approximately 60 species have Based on our molecular and morphological work ( Weststrand bilateral strobili ( Jermy, 1990 ). A few of these have smaller sporo- and Korall, 2016 ), we here propose a revised subgeneric classifi ca- phylls arranged in the same plane as smaller vegetative leaves, a so- tion of Selaginella refl ecting our current knowledge of the evolu- called nonresupinate strobilus, but most species have resupinate tionary relationships of the group. For the classifi cation to be useful strobili, with smaller sporophylls in the same plane as larger vegeta- for future work on Selaginella with respect to research and curation tive leaves
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